plioviverrops is an extinct genus of terrestrial carnivore of the family hyaenidae , endemic to southern europe during the late miocene subepoch ( 11.6 — 5.3 mya ) existing for approximately 6.3 million years .

plioviverrops

el linaje de
plioviverrops
prosperó y dio origen a descendientes con patas más largas y mandíbulas más puntiagudas , similar al aspecto tomado por los cánidos en américa del norte .
the lineage of
plioviverrops
prospered , and gave rise to descendants with longer legs and more pointed jaws , a direction similar to that taken by canids in north america .
= = = auge y desaparición de hiénidos similares a perros = = = los descendientes de
plioviverrops
alcanzaron su apogeo hace 15 millones de años , con más de treinta especies identificadas .
= = = rise and fall of the dog - like hyenas = = = the descendants of
plioviverrops
reached their peak 15 million years ago , with more than 30 species having been identified .
however , other hyaenids soon spread into europe and began spending more time on the ground . the first known european hyaenid was plioviverrops orbignyi , a small critter that has been called a
mongoose - like insectivore / omnivore .
plioviverrops was specialized for eating insects , rather than the wider diet of protictitherium . its claws couldn ' t retract , and it probably spent most of its time on the ground rather than in trees , like this angolan slender mongoose . it lived from 17 million to 5 . 3 million years ago , - - basically all through the miocene epoch .
shortly after the plioviverrops genus evolved , other hyaenids began getting bigger ( along with changes in their teeth ) , as the warm forests and woods of the early miocene epoch opened up into grasslands and open forests with definite seasons . around 10 million years ago , some hyaenids evolved into
running hyenas
who were better adapted to running down their prey like wolves than to crushing bones and scavenging ; others became more like small wolves or jackals , pursuing a scavenging and rodent - hunting lifestyle . finally , between 6 and 7 million years ago , some became fairly slow , bone - crushing animals ( although the spotted hyena can run reasonably fast ) .
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hyaenid
is the proper term for any member of the hyena family ( the hyaenidae ) , including the aardwolf .
only four species of hyaenids still live today , but paleontologists know of at least 69 species from fossils . i cannot hope to describe them all here , so this is kind of a rough overview .
with their heavy jaws and sloping backs , modern hyenas may look vaguely
primitive ,
but in fact the first hyaenid that scientists can recognize as such dates back only between 18 and 17 million years ago - - the early miocene epoch . by that time , horses already had three toes instead of five and cats were recognizable , if only barely .
of course , the ancestors of hyaenids must have separated from those of other carnivores millions of years before . maybe they looked - - and lived - - much like genets such as this small - spotted genet , living in trees much of the time and eating almost anything , including fruit and insects . most of the world was then covered with tropical or subtropical forests , with only a few areas of grassland .
at any rate , that first known hyena is protictitherium gaillardi , which still basically looked like a genet or civet . it could retract its claws like a cat and spent much if not most of its time in the trees . its diet may have been birds , small mammals and even insects .
there were several species of protictitherium after p . gaillardi . even though they were quite primitive , they managed to survive in the trees above their more advanced kin for millions of years , at last dying out between 5 . 3 and 4 . 2 million years ago .
belong ) . they evolved larger and heavier teeth , but we know very little about them , because as yet we have only fragmentary skulls , jaws and teeth of them .
one of the most extreme bone - crushers that ever evolved was adcrocuta eximia which lived in greece , austria and spain a bit more than 9 million years ago . with its thick , short legs , it was not a good runner - - but it was a good bone - crusher and may have thus lived mainly by scavenging , even more so than any modern hyena .
three hyena genera took up running down prey for a living : chasmaporthetes , lycyaena and hyaenictis . they had a long reign as important predators . chasmaporthetes crossed the bering land bridge during the pliocene to enter north america , where it evolved a new species , chasmaporthetes ossifragus - - the only native hyaenid that north america ever had . it did not die out until the first ice ages began , in the pleistocene - - perhaps a victim of the climate changes that also triggered the growth of the great ice sheets .
by the end of the miocene , hyaenids apparently ran into problems . we don ' t know why for sure , but competition with the canids ( wolves , foxes , jackals and other wild
dogs
) may have been part of it . the canids evolved in north america , but they entered eurasia seven million years ago and began to diversify . between three and four million years ago - - the pliocene - - the first wolf - sized canids arrived . whatever the cause , the entire hyaenid family almost died out in europe , except for a few running hyenas like chasmaporthetes and a giant version of the spotted hyena , called the
cave hyena
.
two known genera of hyenas explored a whole new ecological niche - - tongxinictis and tungurictis . they may have been evolving to become like modern civets . their teeth lost all ability to crush bone . but apparently this unique direction didn ' t work out , because they seem to have been rare and soon became extinct .
the aardwolf , a termite - eating hyaenid , must have split off from other hyaenids very early , because its weak jaws and feeble teeth are so different . but there are no hyaenid fossils that seem related . oddly , its coat is colored just like the striped hyena ' s . this may mean the coat coloring is a very old one for hyenas and was shared by the earliest hyaenids .
by the time the climate had truly warmed after the last ice age , perhaps 10 , 000 years ago , only today ' s four species of hyaenids still survived . of them all , only the striped hyena still ranges outside of africa . even the giant cave hyena of europe became extinct . the hyaenid family appears to be in a state of irreversible decline , though the surviving species may well persist and evolve for millions of years longer if humans do not exterminate them .
the hyaenid specialist group ' s page on ancient hyenas , which is more up to date .
koepfli kp , jenks sm , eizirik e , zahirpour t , van valkenburgh b , wayne rk . molecular systematics of the hyaenidae : relationships of a relictual lineage resolved by a molecular supermatrix . molecular phylogenetics and evolution . 2006 mar 31 ; 38 ( 3 ) : 603 - 20 . ( what are these strange numbers and letters ? )
turner a , antón m . evolving eden : an illustrated guide to the evolution of the african large - mammal fauna . columbia university press ; 2004 .
wang x , tedford rh , antón m . dogs : their fossil relatives and evolutionary history . columbia university press ; 2010 .
werdelin l , solounias n . the evolutionary history of hyaenas in europe and western asia during the miocene . bernor , raymond louis , volker fahlbusch , and hans - walter mittmann , in the evolution of western eurasian neogene mammal faunas . columbia university press , 1996 .
angolan slender mongoose - - wikimedia commons , original photo taken by hans hillewaert and released under the creative commons attribution - share alike 3 . 0 unported license .
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. . . 1 . 0 ma , france ) and untermassfeld ( ca . 1 . 0 , germany ) , among others ( turner et al . , 2008 ; palmqvist et al . , 2011 and references therein ) . the well - calibrated last appearance of this species is precisely layer evt7 of the vallparadís section ( fig . 5i ; ca . . . .
. . . during the late pleistocene cave hyenas were the main non - anthropic accumulators of bone remains in caves ( fosse , 1997 ; diedrich , 2014 ) . as a consequence of its activity , hundreds of accumulations have been documented in european caves ( fosse , 1997 ; fosse et al . , 1998 ; diedrich and žák , 2006 ; turner et al . , 2008 ; fourvel , 2012 ; diedrich , 2014 ; fourvel et al . , 2014 ) . in the late pleistocene of the iberian peninsula , the cave hyena was a common element in large mammal assemblages , being recorded from numerous sites ( varela , 2011 ) . . . .
. . . the cave hyena enjoyed notable success , becoming a ubiquitous taxon in european faunal associations of the late pleistocene from the urals to the iberian peninsula ( figure 15 , appendix 7 ) ( carrión et al . , 2006 , stuart andlister , 2014 ) . some authors hold that there are anatomical differences that are not sufficient for making a taxonomic distinction between individuals from the eurasian pleistocene and those from africa ( turner et al . , 2008 ) . results of studies of ancient dna of these fossil remains suggest that the populations of european spotted hyena are a subset of the african population and not a distinct species ( rohland et al . , 2005 ) . . . .
. . . in the last years , actuo - taphonomic studies show that crocuta crocuta seldom creates large accumulations of bones despite having the ability . on the contrary , it is thought that the cave hyena made large accumulations of bones during the late pleistocene throughout europe ( turner et al . , 2008 ; see references in diedrich , 2014 ; fosse , 1997 ; fourvel , 2012 , fourvel et al . , 2015 ) . therefore , apart from the morphological differences between c . spelaea and c . crocuta , ethological differences might exist as well . . . .
. . . given the lack of these diagnostic features of the type species of the genus , the inclusion of this species in hyaenictis is questionable ( being here referred to as ? hyaenictis wehaietu ) . hyaenictis has been classically included in the cursorial hyaenid ecomorphotype ( werdelin and solounias 1996 ; turner et al . 2008 ) , given the lack of the typical durophagous adaptations of adcrocuta . in this paper , we describe a new skull with associated mandible and atlas from the late vallesian of the vallès - penedès basin that , based on the retention of p1 and m2 , as well as the reduced m1 metaconid , is attributed to hyaenictis . . . .
. . . overall , the dentition of ips62078 is more slender ( it displays relatively narrower premolars ) than adcrocuta eximia ( see solounias 1990 , 1991 ; turner et al . 2008 ) . ips62078 further differs from a . eximia in the larger p4 protocone , the presence of a p3 mesial accessory cusp , the longer and tricuspid m1 talonid ( instead of bicuspid , as adcrocuta lacks the hypoconulid ) , and the retention of m2 . . . .
. . . the dentition of the described specimen also does not resemble that of chasmaporthetes , which is characterized by more slender and trenchant premolars with well - developed distal accessory cusps , as well as several more derived features that are absent in hyaenictis spp . ( turner et al . 2008 ) . thus , ips62078 differs from chasmaporthetes ( see kurtén and werdelin 1988 ; werdelin and solounias 1991 ; werdelin and turner 1996 ; antón et al . 2006 ; tseng et al . 2013 ) in the presence of p1 , the relatively broader cheek teeth , the less developed accessory cusps in the premolars , the mesial and distal accessory cusps of the premolars aligned with the main cusp ( instead of lingually tilted ) , the presence of metaconid ( even if vestigial ) , the tricuspid m1 talonid ( chasmaporthetes lacks the hypoconulid and sometimes the hypoconid ) , and the presence of m2 . . . .
. . . according to the ecological opportunity hypothesis , this will be more likely if the immigrant has a substantially different ecology ( e . g . using otherwise unexploited resources ) , or if the continent is poor of species with similar ecologies . for instance , a phylogenetic study suggests that rat snakes ( colubridae : tribe lampropeltini ) underwent an explosive diversification in north america after migrating from eurasia through the bering land bridge [ 14 ] . this pattern is interpreted as the outcome of the colonization of a continent where ecological opportunities were plentiful , since the existing diversity of snakes in north america at the time of immigration was relatively low [ 14 ] . . . .
. . . for instance , a phylogenetic study suggests that rat snakes ( colubridae : tribe lampropeltini ) underwent an explosive diversification in north america after migrating from eurasia through the bering land bridge [ 14 ] . this pattern is interpreted as the outcome of the colonization of a continent where ecological opportunities were plentiful , since the existing diversity of snakes in north america at the time of immigration was relatively low [ 14 ] . likewise , a phylogeny of muroid rodents suggests that a rapid radiation characterized by a burst in speciation rates , followed the arrival to south america [ 15 ] . . . .
. . . their biochronological significance remains , however , relatively limited since their presence in western europe covers a large timeframe . pachycrocuta brevirostris appeared in europe at the beginning of the late villafranchian ( olivola fu / mnq18 , e . g . turner et al . , 2008 ; rook and martínez - navarro , 2010 ) and disappeared at the beginning of the middle galerian , perhaps as a result of the arrival of crocuta ( palombo et al . , 2008 ) . panthera onca gombaszoegensis and canis mosbachensis are present in western and central europe respectively from mnq18 and mnq19 and up to the late galerian ( e . g . . . .
. . . pachycrocuta brevirostris appeared in europe at the beginning of the late villafranchian ( olivola fu / mnq18 , e . g . turner et al . , 2008 ; rook and martínez - navarro , 2010 ) and disappeared at the beginning of the middle galerian , perhaps as a result of the arrival of crocuta ( palombo et al . , 2008 ) . panthera onca gombaszoegensis and canis mosbachensis are present in western and central europe respectively from mnq18 and mnq19 and up to the late galerian ( e . g . . . .
. . . hunting ( or cursorial ) hyenas were the last ecomorphotype to become extinct , being substituted by canids during the pliocene , after the dispersal of the latter into the old world by the end of the miocene ( werdelin and turner 1996a , b ; turner et al . 2008 ) . three out of the four extant hyaenids belong to the bone - cracking ecomorphotype : crocuta crocuta ( erxleben , 1777 ) , hyaena hyaena ( linnaeus , 1758 ) , and parahyaena brunnea ( thunberg , 1820 ) . . . .
. . . more recently , studies on the internal cranial anatomy of hyaenids relied on extant taxa ( holekamp et al . 2007a ; arsznov et al . 2010 ; sakai et al . 2011 ) , so that the brain morphology of extinct bone - cracking hyenas remains undescribed . here , with the aid of ct - scans , we describe the internal cranial morphology ( frontal sinuses and brain ) of the extinct bone - cracking hyena pliocrocuta perrieri , which is the most common hyena in late pliocene to early pleistocene mammalian faunas from europe ( turner et al . 2008 ) . we analyze three complete crania of this hyaenid species from the iberian peninsula , whose external morphology was previously described by vinuesa et al . ( 2014 ) . . . .
. . . alan . cooper @ urltoken 1 these authors contributed equally to this work . types and fill a surprisingly wide range of ecological niches , and their presence is a useful indicator of ecosystem health ( turner et al . 2008 ) . among the four extant species , the spotted hyena , which is the sole member of the genus crocuta , has attracted considerable evolutionary and systematic interest due to having a social system similar to that of many primates , in contrast to other gregarious carnivores ( watts & holekamp 2007 ; diedrich 2008 ; turner et al . 2008 ) . . . .
. . . this diversity was even greater during the quaternary , when hyenids were also present , and the extant carnivore fauna was much more widespread than it is today . however while the evolution of the large african and european terrestrial carnivore guild has had considerably attention ( turner , 1990 ; turner and antón , 1996 , 1998 ; werdelin and lewis , 2005 , 2013 ; turner et al . , 2008 ) , this is less true of asia and southeast ( se ) asia in particular . southeast asia , especially the sundaic and indochinese parts of the indomalayan realm ( encompassing the area from southern china in the north to java in the south , sumatra in the west and borneo and the philippines in the east ; fig . . . .
. . . the earliest record of this species is from the pliocene of europe , ca 5 . 3e3 . 4 ma ( turner et al . , 2008 ) . in se asia its earliest record is kao pah nam , thailand ( recorded as crocuta sp . ) , a currently undated , but probably middle pleistocene , site . . . .
our research during the last 20 years has been chiefly concerned with aspects of the evolution of miocene - pliocene carnivora . areas of particular interest include the functional anatomy and systema…
[ more ]
as an international research team , we strive to understand the anatomy and paleoecology of the once widespread fossil ailurids ( red pandas ) .
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new viverrid , felid , mustelid and amphicyonid fossils from the lothidok formation of west turkana .
recent studies have found regularities in the pattern of distribution of dental parameters such as canine or carnassial length among sympatric carnivores . these regularities are taken to be indicative of community - wide character displacement . this study documents similar patterns in late miocene and earliest pliocene hyaenids from several localities in eurasia and africa . statistical tests . . . [ show full abstract ]
the topotypic material of the giant late miocene hyaenid allohyaena kadici kretzoi is described . new data on the deciduous dentition shows unambiguously that a . kadici is a hyaenid and not a percrocutid as reported by some previous authors . a . kadici is compared to the large hyaenids adcrocuta eximia and crocuta crocuta . these comparisons show that a . kadici has a mixture of primitive . . . [ show full abstract ]
sabre - toothed felids , the machairodontines , have attracted much attention among palaeontologists for many decades , not only because of their spectacular morphology but also because they are a striking example of convergent evolution that is most probably linked to strong selective pressures . in this paper we provide a summary of the changing interpretations of their functional anatomy and . . . [ show full abstract ]
functional anatomy of the forelimb in promegantereon * ogygia ( felidae , machairodontinae , smilodonti . . .
we examine the functional anatomy of the forelimb in the primitive sabre - toothed cat promegantereon ogygia in comparison with that of the extant pantherins , other felids and canids . the study reveals that this early machairodontine had already developed strong forelimbs and a short and robust thumb , a combination that probably allowed p . ogygia to exert relatively greater forces than extant . . . [ show full abstract ]
“earliest zanclean age for the colombacci and uppermost di tetto formations of the « latest messinian » northern apennines : new palaeoenvironmental data from the maccarone section ( marche province , italy ) ” by popescu et al . ( 2007 ) geobios 40 ( 359–373 )
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we review the larger pattern of appearance of the hyaenidae in europe and outline their part in the turnover of the guild of larger carnivora that occurs across the miocene–pliocene boundary . the earliest record of the family is in mn4 , although the patchy nature of the earliest records makes it difficult to be certain about the continent of origin . there is a clear pattern of morphological evolution over that long timespan , from the earliest viverrid - and herpestid - like forms through dog - like and more cursorial taxa to the larger , bone - crunching animals of the later miocene and the pliocene–pleistocene epochs . miocene dog - like hyaenas may indicate that social hunting had emerged by that time , while the appearance of larger species means that hyaena - accumulated bone assemblages may potentially occur in any late miocene to pleistocene locality .
nous révisons le modèle d’apparition des hyaenidae en europe et nous soulignons leur rôle dans le renouvellement des communautés de grands carnivores au cours du miocène et du pliocène . le premier enregistrement de cette famille est situé dans la mn4 , même si la rareté des premiers enregistrements ne permet pas d’établir avec certitude leur continent d’origine . il existe un modèle clair d’évolution morphologique pendant cette période , des premières formes apparentées aux viverridés et aux herpestidés en passant par des formes de type dog - like et des taxons plus cursoriaux , jusqu’aux grands animaux broyeurs d’os du miocène terminal et du plio - pléistocène . les hyènes miocènes qualifiées de dog - like peuvent indiquer que la chasse sociale , en groupe , ait émergé à cette époque , alors que l’apparition des espèces de grande taille signifie que les hyènes accumulatrices de vestiges osseux , ont pu potentiellement exister dans les localités du miocène terminal au pliocène .
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view nexus file : hyaenidae _ werdelin _ & _ solounias _ 1991 . nex
werdelin , l . and n . solounias . 1991 . the hyaenidae : taxonomic systematics and evolution . fossils and strata 30 : 1 - 104 .
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( 53093 ) p . j . wagner and g . f . estabrook 2014 . trait - based diversification shifts reflect differential extinction among fossil taxa proceedings of the national academy of sciences 111 ( 46 ) : 16419 - 16424
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( de bonis et al . , 2005 ) ? ] | | - - †
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tseng , z . j . , jin , c . - z . , liu , j . - y . , zheng , l . - t . & sun , c . - k . , 2008 : fossil hyaenidae ( mammalia : carnivora ) from huainan , anhui province , china . –vertebrata palasiatica : vol . 46 , # 2 , pp . 133 - 146
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adcrocuta ( syn . hyena ) , allohyaena , chasmaporthetes ( syn . ailuraena ) , crocuta , hyaena , hyaenictis , hyaenictitherium , ictitherium , leecyaena , lycyaena , miohyaena , pachycrocuta , palinhyaena , pliocrocuta , protictitherium , thalassictis ( syn . palhyaena ) , tungurictis .
j . j . flynn . 1998 . early cenozoic carnivora (
miacoidea
) . in c . m . janis , k . m . scott , and l . l . jacobs ( eds . ) , evolution of tertiary mammals of north america
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nassarius echinatus is a species of sea snail , a marine gastropod mollusk in the family nassariidae , the nassa mud snails or dog whelks .

nassarius echinatus

nassarius echinatus ( a . adams , 1852 ) - overview - encyclopedia of life
explore what eol knows about nassarius echinatus ( a . adams , 1852 ) .
worms - world register of marine species - nassarius echinatus ( a . adams , 1852 )
nassariidae » nassarius echinatus , id : 305042 , shell detail « shell encyclopedia , conchology , inc .
worms - world register of marine species - nassarius ( niotha ) echinatus ( a . adams , 1852 )
nassarius ( niotha ) h . adams & a . adams , 1853 accepted as nassarius duméril , 1805
nassarius quadrasi alba ( var . ) hidalgo , j . g . , 1904
( of nassarius ( niotha ) echinatus ( a . adams , 1852 ) ) cernohorsky w . o . ( 1984 ) . systematics of the family nassariidae ( mollusca : gastropoda ) . bulletin of the auckland institute and museum 14 : 1 - 356 . [ details ]
( of nassarius ( niotha ) echinatus ( a . adams , 1852 ) ) tsuchiya k . ( 2017 ) . family nassariidae . pp . 910 - 917 , in : t . okutani ( ed . ) , marine mollusks in japan , ed . 2 . 2 vols . tokai university press . 1375 pp . [ details ]
nassarius - species dictionary - global : ispot nature - your place to share nature . ispot is a website aimed at helping anyone identify anything in nature . once you ' ve registered , you can add an observation to the website and suggest an identification yourself or see if anyone else can identify it for you .
description up to 3 cm , similar to n . albescens gemmuliferus , but with more widely spaced , spiny nodules arranged in spiral rows . . . .
description up to 3 cm , similar to n . albescens gemmuliferus , but with more widely spaced , spiny nodules arranged in spiral rows . colour variable , white or cream often with orange - brown spots . habitat : rocky or sandy eulittoral and deeper . distribution : indo - pacific . ( richmond , 1997 ) . [ details ]
richmond , m . ( ed . ) ( 1997 ) . a guide to the seashores of eastern africa and the western indian ocean islands . sida / department for research cooperation , sarec : stockholm , sweden . isbn 91 - 630 - 4594 - x . 448 pp . ( look up in imis ) [ details ]
cernohorsky w . o . ( 1984 ) . systematics of the family nassariidae ( mollusca : gastropoda ) . bulletin of the auckland institute and museum 14 : 1 - 356 . [ details ]
( of nassa echinata a . adams , 1852 ) cernohorsky w . o . ( 1984 ) . systematics of the family nassariidae ( mollusca : gastropoda ) . bulletin of the auckland institute and museum 14 : 1 - 356 . [ details ]
( of nassa ( hebra ) echinata a . adams , 1852 ) cernohorsky w . o . ( 1984 ) . systematics of the family nassariidae ( mollusca : gastropoda ) . bulletin of the auckland institute and museum 14 : 1 - 356 . [ details ]
( of nassa quadrasi var . alba hidalgo , 1904 ) cernohorsky w . o . ( 1984 ) . systematics of the family nassariidae ( mollusca : gastropoda ) . bulletin of the auckland institute and museum 14 : 1 - 356 . [ details ]
tsuchiya k . ( 2017 ) . family nassariidae . pp . 910 - 917 , in : t . okutani ( ed . ) , marine mollusks in japan , ed . 2 . 2 vols . tokai university press . 1375 pp . [ details ]
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tan siong kiat and henrietta p . m . woo , 2010 preliminary checklist of the molluscs of singapore ( pdf ) , raffles museum of biodiversity research , national university of singapore .
tan , k . s . & l . m . chou , 2000 . a guide to the common seashells of singapore . singapore science centre . 160 pp .
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the star system calculates the number of pieces that were handled by conchology , inc . in the last 15 years :
we want to point out that the star system is only very reliable for philippine shells only , as we handle very few foreign shells in general . as time goes , the system will become more and more performant .
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cernohorsky w . o . ( 1984 ) . systematics of the family nassariidae ( mollusca : gastropoda ) . < i > bulletin of the auckland institute and museum < / i > 14 : 1 - 356 .
cernohorsky , w . o . ( 1984 ) systematics of the family nassariidae ( mollusca : gastropoda : i > bulletin of the auckland institute and museum < / i . 14 : 1 - 356
richmond , m . ( ed . ) ( 1997 ) . a guide to the seashores of eastern africa and the western indian ocean islands . sida / department for research cooperation , sarec : stockholm , sweden . isbn 91 - 630 - 4594 - x . 448 pp .
tsuchiya k . ( 2017 ) . family nassariidae . pp . 910 - 917 , in : t . okutani ( ed . ) , < i > marine mollusks in japan < / i > , ed . 2 . 2 vols . tokai university press . 1375 pp .
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the big-eared horseshoe bat ( rhinolophus macrotis ) is a bat species within the rhinolophidae native to china , india , indonesia , laos , malaysia , nepal , pakistan , the philippines , thailand , and vietnam .

big - eared horseshoe bat

complete mitochondrial genome of the big - eared horseshoe bat rhinolophus macrotis ( chiroptera , rhinolophidae ) .
complete mitochondrial genome of the big - eared horseshoe bat rhinolophus macrotis ( chiroptera , rhinolophidae ) . - pubmed - ncbi
big - eared horseshoe bat or rhinolophus macrotis is listed on the iucn red list ( 1996 ) as lower risk / least concern .
a young / baby of a bigeared horseshoe bat is called a ' pup ' . a bigeared horseshoe bat group is called a ' colony or cloud ' .
the big - eared horseshoe bat is listed as least concern ( lr / lc ) , lowest risk . does not qualify for a more at risk category . widespread and abundant taxa are included in this category , on the iucn red list of threatened species
in china , 79 individuals of big - eared horseshoe bat complex were sampled during 2006–2012 from 14 localities ( fig . 1 and table s1 , supporting information ) , including the 12 specimens of the 7 small form and 5 large form bats published previously 18 . all bats were identified following csorba et al . 19 .
how to cite this article : sun , k . et al . the complex evolutionary history of big - eared horseshoe bats ( rhinolophus macrotis complex ) : insights from genetic , morphological and acoustic data . sci . rep . 6 , 35417 ; doi : 10 . 1038 / srep35417 ( 2016 ) .
pleistocene climatic fluctuations and accompanying ecological changes in china have presented severe challenges to the survival of bat species , greatly affecting their population differentiation and contemporary distribution 3 , 21 , 22 . in this study , the tmrca of the entire r . macrotis complex populations dated to 1 . 51 ma . during this period , china was experiencing glacial - interglacial cycles , including the poyang glacial stage ( 1 . 8 ma ) and the dagu glacial stage ( 1 . 1 ma ) 23 . climatic changes and temperature decline may have forced the big - eared horseshoe bats to diverge from other bat species and evolve separately .
we sequenced and characterized the complete mitochondrial genome of the big - eared horseshoe bat , rhinolophus macrotis . total length of the mitogenome is 16 , 848 bp , with a base composition of 31 . 2 % a , 25 . 3 % t , 28 . 8 % c and 14 . 7 % g . the mitogenome consists of 13 protein - coding genes , 2 rrna ( 12s and 16s rrna ) genes , 22 trna genes and 1 control region . it has the same gene arrangement pattern as those of typical vertebrate mitochondrial genome . the results will contribute to our understanding of the taxonomic status and evolution in the genus rhinolophus bats .
in our previous study 18 , the large and small forms were identified from sympatric large - eared horseshoe bats in china , suggesting the existence of a cryptic species . in this study , three sympatric populations ( gd1 , hun and jx1 ) were detected between small and large forms ( fig . 1 ) , suggesting secondary contact after putative speciation .
we used a uniq - 10 column animal genomic dna isolation kit ( sangon , china ) to extract total genomic dna from collected bat wing membranes which had been preserved in 99 % ethanol .
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the mainland populations probably represent two distinct species . the philippine form of r . macrotis was initially described as a separate species , r . hirsutus ( anderson , 1905 ) , but was later subsumed under r . macrotis by tate ( 1943 ) but hirsutus is morphologically and genetically distinct ( guillen et al . in csorba et al . 2003 ) .
hutson , a . m . , racey , p . a . ( chiroptera red list authority ) & cox , n . ( global mammal assessment team )
justification : listed as least concern in view of its wide distribution , presumed large population , and because it is unlikely to be declining fast enough to qualify for listing in a more threatened category .
though this species is widely distributed in its range in south asia it is known from a few localities and has a small colony size . the population size of this species is low and a declining trend in the population is inferred ( molur et al . 2002 ) . in peninsular malaysia and southern thailand it is rare in tall lowland forest and also hill forest in peninsular malaysia ( bumrungsri and francis pers . comm . 2006 ) and widespread but seemingly uncommon in the philippines ( heaney et al . 1998 ) .
in south asia , the habitat of this species is being deforested for timber , firewood and conversion for agricultural use . in nepal it is threatened due to increase in tourism leading to disturbance to roosting sites ; fumigation and chemical pesticides to rid the caves of roosts ( t . k . shreshta pers . comm . january 2002 ; molur et al . 2002 ) . in southeast asia , it is probably threatened in parts of its range ( such as malaysia ) by ongoing habitat loss .
in south asia , there are no direct conservation measures in place for this species . the species has not been recorded from any protected areas . additional studies are needed into the distribution , abundance , breeding biology , general ecology and threats to this little - known species . populations should be monitored to record changes in abundance and distribution . habitat maintenance , conservation and restoration are needed . public awareness activities need to be taken up to mitigate any further threats to this taxon ( molur et al . 2002 ) . in view of its wide range in southeast asia , it seems probable that the species has been recorded from some protected areas , although this needs to be confirmed .
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( a ) phylogenetic tree based on the analysis of the combined mitochondrial cyt b and control region . numbers above the branches are bootstrap support from in maximum likelihood followed by posterior probabilities from bayesian analyses . ( b ) sampling sites for the mt lineages included in the study . circle sizes are proportional to the number of individuals captured . abbreviations of samples populations are indicated in table s1 . the map was made with qgis 2 . 8 ( urltoken ) and natural earth public domain map data ( urltoken ) , and modified in illustrator .
for 79 individuals in the r . macrotis complex sampled from 14 localities across the entire chinese range of the species , we found much variation in cyt b ( 1 , 140 bp ) and control region ( 464 bp ) . a total of 29 haplotypes of cyt b were defined based on 103 polymorphic sites ( 71 of which were parsimony informative ) . no insertions or deletions were found . fifty haplotypes of the control region were defined based on 115 polymorphic sites ( 90 of which were parsimony informative ) . the alignment of the combined cyt b and control region ( 1 , 604 bp ) resulted in 53 haplotypes . for the autosomal chd1 gene ( 742 bp ) , a total of 20 haplotypes were defined from 71 individuals based on 24 polymorphic sites ( 6 of which were parsimony informative ) .
the ranges of the three clades were partially sympatric ( fig . 1b ) . both sxi and cq populations contained individuals from clades 2 and 3 ( all large forms ) , both the hun and jx1 populations contained individuals from clades 1 and 3 , and the gd1 population contained individuals from clades 1 and 2 .
in general , intraspecific genetic divergence levels among bats are typically less than 2 % within cyt b 20 . thus we used cyt b to calculate the intra - lineage and inter - lineage genetic differences . in this species complex , the maximum level of uncorrected intra - clade divergence was ≤2 % ( table 1 ) . among the three clades , the minimum uncorrected divergence was over 2 % ( table 1 ) , though never exceeded 4 % .
since the clades were distinct genetic pools , population genetics analyses were performed within each lineage . genetic diversity was highest in clade 1 , followed by clades 3 and 2 for both the cyt b and control region ( table 2 ) .
we estimated divergence times among clades using cyt b ( table 3 ) . the inferred tmrca for all r . macrotis complex was 1 . 51 ma ( million years ago ) , with similar divergence times mt clades 1 and 2 ( 0 . 64 and 0 . 66 ma , respectively ) . in contrast , mt clade 3 originated much later . tajima’s d values and fu’s fs tests indicated that none of the three mt lineages deviated significantly from neutrality ( table 4 ) . unlike in mt clades 2 and 3 , analysis of mt clade 1 failed to reject the model of population expansion ( table 4 ) , with an estimated timing of expansion occurring 78 . 8 ka ( thousand years ago ) ( 95 % ci : 38 . 1–96 . 1 ka ) .
consistent with the microsatellite results , the large form individuals from mt clade 2 and mt clade 3 did not form independent chd1 haplogroups and instead shared five haplotypes ( fig . 3 ) . however , the large form and the small form had their own distinct haplotypes with one exception ( fig . 3 ) .
colours indicate the membership of each mt lineage , including clade 1 ( red ) , clade 2 ( green ) and clade 3 ( blue ) .
we focused on the geographic pattern of nuclear genetic variation within mt clades 2 and 3 , as the above analyses failed to detect their genetic differentiation in individual clustering ( figs 2 and 3 ) . no significant ibd was found within the large forms ( p > 0 . 05 ) . however , when excluding the gd1 population , the test of ibd suggested that the two lineages had not evolved separately but were connected because smooth clinal variation rather than a geographic break was observed in the nuclear genetic variation ( fig . 4 ) .
white circles represent the distances between gd1 population in large forms and other populations .
phenotypic analyses distinguished the large and small forms using either forearm length or resting frequency of echolocation calls ( fig . 5 ) , including in sympatric populations .
circles represent the mean values . colours indicate the membership of each mt lineage , including clade 1 ( red ) , clade 2 ( green ) and clade 3 ( blue ) . the asterisks represent the individuals from gd1 population in large forms .
within the large form , morphological differentiation was not significant between mt clade 2 and mt clade 3 . forearm length was significantly explained by site , but not by sex and mt lineage , or by interactions among variables ( table 5 ) . resting frequency was significantly explained by sex and mt lineage , as well as by site . no significant interaction was found between effects ( table 5 ) .
lineage , sex and site , analyzed by general linear model ( glm ) .
we focused on the geographic pattern of acoustic variation within mt clade 2 / clade 3 of the large form as we found no significant morphological differences between these two clades . we detected positive significant associations between resting frequency and both longitude ( r = 0 . 39 , p = 0 . 0011 ) and latitude ( r = 0 . 284 , p = 0 . 0199 ) . when excluding gd1 , clinal variation was much more significant ( longitude : r = 0 . 48 , p < 0 . 0001 ; rf vs latitude : r = 0 . 74 , p < 0 . 0001 ) .
the tmrcas of the combined mt clade 1 ( small form ) and mt clade 2 ( large form ) dated to 1 . 16 ma , suggesting that the two mt lineages differentiated from each other between 1 . 16–0 . 64 ma . this time was consistent with two major cold glacial stages , xixiabangma glaciations ( 1 . 17–0 . 8 ma ) 24 and the naynayxungla glaciations ( 0 . 71–0 . 59 ma ) 25 . the former stage is one of the coldest recent climatic periods based on a high mass accumulation rate for chinese loess 26 . at that time , the populations might have become isolated into different refugia and occupied different habitats and climate zones either due to , or eventually leading to , local ecological adaptation , and two distinct lineages distributed in central and southwest china .
the mitochondrial genetic analyses indicated that large forms diverged into two distinct lineages , clade 2 and clade 3 with a level of divergence similar to that between the small and large forms . additionally , these two mt clades show distinct geographic distribution , with clade 2 primarily occurring central china , whereas clade 3 is primarily in southeast china ( fig . 1 ) , although there is sympatry in two localities ( cq and sxi ) . these results suggest a cryptic mitochondrial lineage in the large form in china .
an increasing number of studies have reported mitochondrial species - level paraphyly ( e . g . refs 6 , 7 and 8 ) . in our study , phylogenetic analyses revealed that mt clade 1 ( small forms ) was nested within the mt clades 2 + 3 group ( large forms ) , rendering large forms paraphyletic with respect to small forms . two evolutionary processes may account for this mitochondrial paraphyly : ( i ) incomplete lineage sorting and the persistence of highly divergent mt lineages , and ( ii ) mitochondrial introgression .
based on our analyses of population demographic history , the small form might have undergone post - glacial range expansion after the baiyu ( the last ) glaciation 24 , following secondary contact with the large forms . in the mitochondrial trees , all individuals from the three sympatric areas diverged recently ( see the top of mt clade 1 ; figs s1 and s2 ) . moreover , the number of small forms is less than large forms in three sympatric areas ( fig . 1 ) , suggesting the small form may be expanding into areas occupied by the large form .
sampling sizes were different for morphological characters , echolocation calls , mtdna , microsatellite dna and the chd1 gene . for morphological characters ( forearm length ) , 133 independent samples were measured . for echolocation calls , 109 independent samples were recorded . from those individuals with morphological and echolocation data , 79 samples were sequenced for mtdna , 78 and 71 were examined using microsatellite dna and chd1 analyses , respectively . for each sampling locality , we determined the latitude and longitude using gps ( etrex vista ) and then calculated the geographic distance matrixes among localities .
eight microsatellite loci , reffer 15 , 22 , 24 , 27 , h3 , pd3 , a4 and ph69a , were amplified using fluorescently labeled primers for 78 individuals . primer sequences and pcr conditions followed those of rossiter et al . 45 and hua et al . 46 . amplified pcr products were analyzed using the abi 3730 automated dna sequencer . the resulting sequences were analyzed using genemapper id 3 . 2 ( applied biosystems ) . all loci were screened for null alleles and large allele dropouts using micro - checker v2 . 2 . 3 47 . tests for deviation from hardy - weinberg equilibrium and linkage disequilibrium were performed for each population in genepop v4 . 0 48 .
the autosomal chd1 gene was amplified using two sets of primers ( ex26f and ex27r ; emb26f and emb27r ) 49 because some individuals failed to amplify with one set , and so we tried a second set . for the first set of primers , the pcr conditions were an initial denaturation at 95 °c for 5 min , followed by 36 cycles of denaturation at 94 °c for 30 s , annealing at 63 °c for 30 s , and extension at 70 °c for 2 min 30 s , and a final extension at 72 °c for 10 min . for the second set , the pcr conditions were 35 cycles of denaturation at 94 °c for 45 s , annealing at 59 °c for 45 s , and extension at 72 °c for 1 min . heterozygous sites in chd1 sequences were resolved to two haplotypes per individual using phase 2 . 1 50 implemented in dnasp v5 51 .
haplotype diversity ( h ) and nucleotide diversity ( π ) were calculated for mitochondrial cyt b and control region for each population and mt lineage . the uncorrected cyt b genetic distances within and among mt lineages were calculated in mega 5 . 05 52 . for microsatellites , expected heterozygosity ( h e ) and observed herterozygosity ( h o ) were calculated using genepop , and mean allele number and allelic richness for per locus and per taxon was assessed in fstat 2 . 9 . 3 53 . for the chd1 gene , π , h e and h o for each taxon was calculated using arlequin v3 . 5 54 .
we calculated nuclear genetic distances between localities using slatkin’s linearized f st ( given by f st / ( 1 − f st ) ) . an isolation by distance ( ibd ) model was estimated from the large forms based on microsatellites .
we used jmodeltest 61 and the akaike information criterion to select the best model of evolution for ml and bi analyses . the best - fit models were as follows : ( 1 ) trn + g [ g = 0 . 072 ] for cyt b , ( 2 ) tim3 + i + g [ i = 0 . 478 ; g = 0 . 507 ] for control region , trn + i + g [ i = 0 . 651 ; g = 0 . 714 ] for the combined mtdna data . for ml analysis , the starting tree was obtained with bionj 62 and we evaluated support of the resulting topologies using 1 , 000 nonparametric bootstraps . for bi analysis , we used the molecular evolution model parameters estimated for each data set and two simultaneous runs of markov chain monte carlo ( mcmc ) analysis , each comprising four chains and 10 6 generations . trees and parameters were sampled every 10 generations . when the run terminated , the deviation of split frequencies reached a value < 0 . 01 . the ln - likelihoods of trees reached an asymptote . the first 25 % of the sampled trees were discarded as a burn - in .
geographic variation for phenotypic characters was explored via box plots , with longitude and latitude on the abscissa . the relationship of resting frequency to either longitude or latitude was estimated by linear regression analysis , with averaging of frequency by site .
to estimate the phenotypic differentiation between mt clade 2 and mt clade 3 in the large form , we used a general linear model with type iii sums of squares to test for an effect of sex , site and mt lineage on forearm length and echolocation frequency . all variables were treated as fixed effects in the model .
accession codes : all sequence data has been uploaded to genbank ( kx261888 - kx261966 , kx826057 - kx826076 ) . microsatellite genotypes , sequence alignments by markers , phylogenetic trees and morphological and acoustic data files are uploaded on the dryad digital repository ( doi : 10 . 5061 / dryad . b1c88 ) .
( eds . ) ] [ 339–361 ] ( academic press , new york , 2003 ) .
( eds . ) ] ( cornell university press , new york , 1996 ) .
fstat , a program to estimate and test gene diversities and fixation indices ( version 2 . 9 . 3 ) . updated from goudet ( 1995 ) . available at :
arlequin suite ver 3 . 5 : a new series of programs to perform population genetics analyses under linux and windows
populations 1 . 2 . 30 : population genetic software ( individuals or population distances , phylogenetic trees ) ( 2007 ) .
genetix 4 . 05 , logiciel sous windows tm pour la génétique des populations . laboratoire génome , populations , interactions , cnrs umr 5171 , université de montpellier ii , montpellier ( 1996–2004 ) .
we thank lei wang , yuyan you , sen liu , shi li , guanjun lu , limin shi and xu zhu for field support . this work was financed by the national natural science foundation of china ( grant nos . 31370399 , 31270414 and 31570390 ) , the specialized research fund for the doctoral program of higher education ( no . 20120043130002 ) , the fundamental research funds for the central universities ( no . 2412016kj045 ) and the program for introducing talents to universities ( b16011 ) .
k . s . designed the study , performed much of the sampling , implemented most of genetic methodologies and analyses , and wrote the manuscript . r . t . k . assisted with interpretation of data and gave important comments on multiple versions of the manuscript . t . l . and x . w . contributed part of genetic methodologies . l . j . , t . j . and a . l . assisted with sample collection . j . f . assisted with study design , provided laboratory space , reagents , and some funding . all authors reviewed the manuscript .
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simmons , nancy b . / wilson , don e . , and deeann m . reeder , eds .
mammal species of the world : a taxonomic and geographic reference , 3rd ed . , vols . 1 & 2
mammal species of the world : a taxonomic and geographic reference , 2nd ed . , 3rd printing
with contributions by bernadette n . graham , adam p . potter , and mariana m . upmeyer
comments : philippinensis species group . includes episcopus and hirsutus ; see ellerman and morrison - scott ( 1951 ) , tate ( 1943 ) , corbet and hill ( 1992 ) , and bates and harrison ( 1997 ) , but also see ingle and heaney ( 1992 ) , who suggested that hirsutus may deserve recognition as a distinct species . does not include siamensis , see francis et al . ( 1999b ) and hendrichsen et al . ( 2001b )
disclaimer : itis taxonomy is based on the latest scientific consensus available , and is provided as a general reference source for interested parties . however , it is not a legal authority for statutory or regulatory purposes . while every effort has been made to provide the most reliable and up - to - date information available , ultimate legal requirements with respect to species are contained in provisions of treaties to which the united states is a party , wildlife statutes , regulations , and any applicable notices that have been published in the federal register . for further information on u . s . legal requirements with respect to protected taxa , please contact the u . s . fish and wildlife service .
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mitochondrial dna a dna mapp seq anal . 2016 nov ; 27 ( 6 ) : 4078 - 4079 . epub 2015 jan 21 .
a jilin provincial key laboratory of animal resource conservation and utilization , northeast normal university , changchun , china .
picture has been licensed under a creative commons attribution sharealike license original source : base map derived from file : blankmap - world . png . distribution data from iucn red list author : chermundy
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to cite this page : myers , p . , r . espinosa , c . s . parr , t . jones , g . s . hammond , and t . a . dewey . 2018 . the animal diversity web ( online ) . accessed at https : / / animaldiversity . org .
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